Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

The balance between RuBP carboxylation and RuBP regeneration: a mechanism underlying the interspecific variation in acclimation of photosynthesis to seasonal change in temperature

Yusuke Onoda A B D , Kouki Hikosaka A and Tadaki Hirose A C
+ Author Affiliations
- Author Affiliations

A Graduate School of Life Sciences, Tohoku University, Aoba, Sendai, 980-8578 Japan.

B Current address: Department of Plant Ecology, Utrecht University, PO Box 800.84 3508 TB Utrecht, The Netherlands.

C Department of International Agriculture Development, Tokyo University of Agriculture, Sakuragaoka 1-1-1, Setagaya, Tokyo, 156-8502 Japan.

D Corresponding author. Email: Y.Onoda@bio.uu.nl

Functional Plant Biology 32(10) 903-910 https://doi.org/10.1071/FP05024
Submitted: 31 January 2005  Accepted: 20 May 2005   Published: 5 October 2005

Abstract

The ratio of the capacities of ribulose-1,5-bisphosphate (RuBP) regeneration to RuBP carboxylation (Jmax / Vcmax) (measured at a common temperature) increases in some species when they are grown at lower temperatures, but does not increase in other species. To investigate the mechanism of interspecific difference in the response of Jmax / Vcmax to growth temperature, we analysed the temperature dependence of Vcmax and Jmax in Polygonum cuspidatum and Fagus crenata with the Arrhenius function. P. cuspidatum had a higher ratio of Jmax / Vcmax in spring and autumn than in summer, while F. crenata did not show such change. The two species had a similar activation energy for Vcmax (EaV) across seasons, but P. cuspidatum had a higher activation energy for Jmax (EaJ) than F. crenata. Reconstruction of the temperature response curve of photosynthesis showed that plants with an inherently higher EaJ / EaV (P. cuspidatum) had photosynthetic rates that were limited by RuBP regeneration at low temperatures and limited by RuBP carboxylation at high temperatures, while plants with an inherently lower EaJ / EaV (F. crenata) had photosynthetic rates that were limited solely by RuBP carboxylation over the range of temperatures. These results indicate that the increase in Jmax / Vcmax at low growth temperatures relieved the limitation of RuBP regeneration on the photosynthetic rate in P. cuspidatum, but that such change in Jmax / Vcmax would not improve the photosynthetic rate in F. crenata. We suggest that whether or not the Jmax / Vcmax ratio changes with growth temperature is attributable to interspecific differences in EaJ / EaV between species.

Keywords: activation energy, interspecific variation, Jmax, temperature acclimation, Vcmax.


Acknowledgments

We thank Ken-ichi Sato, Toshihiko Kinugasa, Yuko Yasumura and Borjigidai Almaz for help in growing plants, and Onno Muller for comments on the draft manuscript. This study was partly supported by Grant-in-Aid for from JSPS for Young Research Fellows (YO), and from Japan Ministry of Education, Culture, Sports, Science and Technology for KH and TH.


References


Bernacchi CJ, Singsaas EL, Pimentel C, Portis AR, Long SP (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant, Cell & Environment 24, 253–259.

Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology 31, 491–543.
CrossRef |

Bunce JA (2000a) Acclimation of photosynthesis to temperature in eight cool and warm climate herbaceous C3 species: temperature dependence of parameters of a biochemical photosynthesis model. Photosynthesis Research 63, 59–67.
CrossRef |

Bunce JA (2000b) Acclimation to temperature of the response of photosynthesis to increased carbon dioxide concentration in Taraxacum officinale. Photosynthesis Research 64, 89–94.
CrossRef |

Drake BG, Gonzalez-Meler MA, Long SP (1997) More efficient plants — a consequence of rising atmospheric CO2. Annual Review of Plant Physiology and Plant Molecular Biology 48, 609–639.
CrossRef | PubMed |

Dreyer E, Le Roux X, Montpied P, Daudet FA, Masson F (2001) Temperature response of leaf photosynthetic capacity in seedlings from seven temperate tree species. Tree Physiology 21, 223–232.
PubMed |


Ethier GJ, Livingston NJ (2004) On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar–von Caemmerer–Berry leaf photosynthesis model. Plant, Cell & Environment 27, 137–153.
CrossRef |

Evans JR (1987) The relationship between electron transport components and photosynthetic capacity in pea leaves growth at different irradiances. Australian Journal of Plant Physiology 14, 157–170.

Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.
CrossRef |

Farquhar, GD ,  and  von Caemmerer, S (1982). Modelling of photosynthetic response to environmental conditions. In ‘Physiological plant ecology II’. pp. 550–587. (Springer-Verlag: Heidelberg)

Fridlyand LE, Backhausen JE, Scheibe R (1999) Homeostatic regulation upon changes of enzyme activities in the Calvin cycle as an example for general mechanisms of flux control. What can we expect from transgenic plants? Photosynthesis Research 61, 227–239.
CrossRef |

Harrison EP, Olcer H, Lloyd JC, Long SP, Raines CA (2001) Small decreases in SBPase cause a linear decline in the apparent RuBP regeneration rate, but do not affect Rubisco carboxylation capacity. Journal of Experimental Botany 52, 1779–1784.
CrossRef | PubMed |

Hikosaka K (1997) Modelling optimal temperature acclimation of the photosynthetic apparatus in C3 plants with respect to nitrogen use. Annals of Botany 80, 721–730.
CrossRef |

Hikosaka, K (2005). Nitrogen partitioning in the photosynthetic apparatus of Plantago asiatica leaves grown at different temperature and light conditions: similarities and differences between temperatures and light acclimation. Plant and Cell Physiology (In press).

Hikosaka K, Murakami A, Hirose T (1999) Balancing carboxylation and regeneration of ribulose-1,5-bisphosphate in leaf photosynthesis: temperature acclimation of an evergreen tree, Quercus myrsinaefolia. Plant, Cell & Environment 22, 841–849.
CrossRef |

Kirschbaum MUF, Farquhar GD (1984) Temperature dependence of whole-leaf photosynthesis in Eucalyptus pauciflora Sieb. ex Spreng. Australian Journal of Plant Physiology 11, 519–538.

Loreto F, Dimarco G, Tricoli D, Sharkey TD (1994) Measurement of mesophyll conductance, photosynthetic electron transport and alternative electron sinks of field grown wheat leaves. Photosynthesis Research 41, 397–403.
CrossRef |


Medlyn BE, Loustau D, Delzon S (2002a) Temperature response of parameters of a biochemically based model of photosynthesis. I. Seasonal changes in mature maritime pine (Pinus pinaster Ait.). Plant, Cell & Environment 25, 1155–1165.
CrossRef |

Medlyn BE, Dreyer E, Ellsworth D, Forstreuter M, Harley PC , et al. (2002b) Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data. Plant, Cell & Environment 25, 1167–1179.
CrossRef |

Muraoka H, Koizumi H (2005) Photosynthetic and structural characteristics of canopy and shrub trees in a cool-temperate deciduous broadleaved forest: implication to the ecosystem carbon gain. Agricultural and Forest Meteorology (In press) ,

Nie GY, Long SP, Garcia RL, Kimball BA, Lamorte RL, Pinter PJ, Wall GW, Webber AN (1995) Effects of free-air CO2 enrichment on the development of the photosynthetic apparatus in wheat, as indicated by changes in leaf proteins. Plant, Cell & Environment 18, 855–864.

Onoda Y, Hikosaka K, Hirose T (2005) Seasonal change in the balance between capacities of RuBP carboxylation and RuBP regeneration affects CO2 response of photosynthesis in Polygonum cuspidatum. Journal of Experimental Botany 56, 755–763.
CrossRef | PubMed |

Price GD, von Caemmerer S, Evans JR, Siebke K, Anderson JM, Badger MR (1998) Photosynthesis is strongly reduced by antisense suppression of chloroplastic cytochrome bf complex in transgenic tobacco. Australian Journal of Plant Physiology 25, 445–452.

Sage RF (1994) Acclimation of photosynthesis to increasing atmospheric CO2: the gas exchange perspective. Photosynthesis Research 39, 351–368.
CrossRef |

Sharkey TD, Stitt M, Heineke D, Gerhardt R, Raschke K, Heldt HW (1986) Limitation of photosynthesis by carbon metabolism II. O2 insensitive CO2 assimilation results from triose phosphate utilization limitations. Plant Physiology 81, 1123–1129.

Sudo E, Makino A, Mae T (2003) Differences between rice and wheat in ribulose-1,5-bisphosphate regeneration capacity per unit of leaf-N content. Plant, Cell & Environment 26, 255–263.
CrossRef |

Terashima I, Evans JR (1988) Effect of light and nitrogen nutrition on the organization of the photosynthetic apparatus in spinach. Plant & Cell Physiology 29, 143–156.

Theobald JC, Mitchell RAC, Parry MAJ, Lawlor DW (1998) Estimating the excess investment in ribulose-1,5-bisphosphate carboxylase / oxygenase in leaves of spring wheat grown under elevated CO2. Plant Physiology 118, 945–955.
CrossRef | PubMed |

von Caemmerer, S (2000). ‘Biochemical models of leaf photosynthesis.’ (CSIRO Publishing: Melbourne)

von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387.
CrossRef |

Walcroft AS, Whitehead D, Silvester WB, Kelliher FM (1997) The response of photosynthetic model parameters to temperature and nitrogen concentration in Pinus radiata D. Don. Plant, Cell & Environment 20, 1338–1348.
CrossRef |

Wilson KB, Baldocchi DD, Hanson PJ (2000) Spatial and seasonal variability of photosynthetic parameters and their relationship to leaf nitrogen in a deciduous forest. Tree Physiology 20, 565–578.
PubMed |


Wullschleger SD (1993) Biochemical limitations to carbon assimilation in C3 plants: a retrospective analysis of the A / Ci curves from 109 species. Journal of Experimental Botany 44, 907–920.

Yamasaki T, Yamakawa T, Yamane Y, Koike H, Satoh K, Katoh S (2002) Temperature acclimation of photosynthesis and related changes in photosystem II electron transport in Winter wheat. Plant Physiology 128, 1087–1097.
CrossRef | PubMed |

Yamori W, Noguchi K, Terashima I (2005) Temperature acclimation of photosynthesis in spinach leaves: analyses of photosynthetic components and temperature dependencies of photosynthetic partial reactions. Plant, Cell & Environment 28, 536–547.
CrossRef |








Rent Article (via Deepdyve) Export Citation Cited By (46)